Clonal diversity alters the infection dynamics of a malaria parasite (Plasmodium mexicanum) in its vertebrate host

Abstract

Ecological and evolutionary theory predicts that genetic diversity of microparasites within infected hosts will influence the parasite replication rate, parasitemia, transmission strategy, and virulence. We manipulated clonal diversity (number of genotypes) of the malaria parasite, Plasmodium mexicanum, in its natural lizard host and measured important features of the infection dynamics, the first such study for any natural Plasmodium-host association. Hosts harboring either a single P. mexicanum clone or various combinations of clones (scored via three microsatellite markers) were established. Production of asexually replicating stages (meronts) and maximal meront parasitemia did not differ by clonal diversity, nor did timing of first production of transmission stages (gametocytes). However, mean rate of gametocyte increase and maximal gametocyte parasitemia were greater for hosts with mixed-clone infections. Characteristics of infections were more variable in hosts with mixed-clone infections than with single-clone infections except for first production of gametocytes. One or more of the parasite reproductive traits were extreme in 20 of 52 hosts with mixed-clone infections. This was not associated with specific clones, but diversity itself. The overall pattern from studies of clonal diversity for human, rodent, and now reptile malaria parasites confirms that the genetic diversity of infections in the vertebrate host is of central importance for the ecology of Plasmodium.

Virulence of a Malaria Parasite, Plasmodium mexicanum, for Its Sand Fly Vectors, Lutzomyia vexator and Lutzomyia stewarti (Diptera: Psychodidae)

“…), and, to prevent any possible interaction between parasites, only lizards carrying P. mexicanum were used for the infected lizard trials. To obtain control noninfected lizards, animals were collected from sites where malaria has been absent in the lizard population for decades of study (Vardo-Zalik and Schall 2009). Blood smears from these animals were also scanned, with none found infected.…”

Leukocyte Profiles for Western Fence Lizards,Sceloporus occidentalis, Naturally Infected by the Malaria ParasitePlasmodium mexicanum

“…Particularly of interest is any change in the leukocyte population because such changes indicate an immune response initiated by the reptilian host (Bonadiman et al, 2010). Although many hematozoan infections are considered nonpathogenic for their reptilian hosts (Brown et al, 2006;Jacobson, 2007;Sperry et al, 2009;Stacy et al, 2011;Xuereb et al, 2012), some parasites do cause a variety of negative effects, including reduced fecundity, anemia, and reduced weight (Schall, 2002;Ujvari et al, 2004;Amo et al, 2005;Ujvari and Madsen, 2005;Vardo-Zalik and Schall, 2008;Motta et al, 2011). Changes in the leukocyte patterns can greatly affect the overall pathology caused by the parasite, may influence the parasite's infection dynamics in its host, and may predispose an animal to other infectious organisms.…”

“…The western fence lizard, Sceloporus occidentalis, is naturally infected with the hematozoan parasite Plasmodium mexicanum in northern California and has been the focus of study at the Hopland Research and Extension Center since 1978 (Schall, 1983(Schall, , 2002Vardo-Zalik and Schall, 2009). Plasmodium mexicanum is one of the most well studied of the approximately 90 reptilian Plasmodium species; it is a virulent species, affecting the lizard's fecundity, stamina, and blood physiology (hemoglobin and glucose), among other factors (Schall, 2002;Vardo-Zalik and Schall, 2008). The high fitness consequences of this pathogen suggest that lizards would benefit from eliciting an immune response to eliminate, or at least control, infections (Sheldon and Verhulst, 1996), as observed in other malaria-host systems.…”

“…Therefore, any immune response elicited by the lizard may be to reduce, rather than eliminate infection. Although much work has been conducted on the relationship between the parasite and its host (Schall, 1996(Schall, , 2002Schall, 2008, 2009), there has been only one study examining the effect of malaria infection on leukocyte composition in S. occidentalis (McFarland et al, 2012); this work used experimental infections and used only male lizards. A further examination of naturally infected lizards is warranted as the stressors of captivity plus malaria infection could exaggerate the immune response observed in experimental studies (Davis et al, 2008).…”

“…How the immune system reacts to single versus multiclonal infections could also affect our interpretation of parasite infection dynamics, particularly if the immune system has a stronger effect on a certain type of infection or clone within an infection (Read and Taylor, 2001;de Roode et al, 2003). Changes in leukocyte patterns with infection status, or variations in immune status among lizards, may result in the variations in parasite growth rates, and possibly virulence, of the malaria parasite observed in previous experiments on this system (VardoZalik andSchall, 2008, 2009;Kochin et al, 2010;Neal and Schall, 2014). Therefore, determining whether lizards mount an immune response to malaria infection and how that response affects the parasite is critical to further studies on this model wildlife malaria system.…”